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Biophysical Journal Volume 71 September 1996 1348-1349

What is the Surface Tension of a Lipid Bilayer Membrane?

Fritz JAhnig'l
Max-Planck-lnstitut fur Biologie, Abteilung Membranbiochemie, Corrensstrasse 38, D-72076 Tubingen, Germany

In a recent paper in this journal, Chiu et al. (1995) presented

a molecular dynamics study of a planar lipid bilayer membrane in water with the explicit incorporation of a surface
tension. Parallel to the membrane plane, a negative pressure
of -100 atmospheres was applied, derived from the measured surface tension of a monolayer at an air/water interface. The same approach was put forward by Feller et al.
(1995).
The question as to what is the surface tension of a bilayer
membrane goes far back in the literature. To my knowledge,
it was first raised by de Gennes and Papoular in 1969 and
taken up again in a paper by Brochard et al. (1976). The
answer was that bilayer membranes of vesicles or cells
(without concentration gradients across the membrane) have
zero surface tension, because the free energy should be
minimal with respect to the surface area of the membrane.
This explained the great fluctuations in the shape of red cell
membranes. Independently, the same argument was put
forward by Tanford (1979), for membranes without high
curvature, and by Israelachvili et al. (1977). The latter
authors used this argument to develop a theory for the
self-assembly of lipids in micelles or bilayers, either planar
or vesicular, which proved to be very useful. Likewise, a
theory for the exchange of lipid molecules between a bilayer
and a monolayer at the air/water interface was worked out
based on the assumption that the surface tension of a bilayer
is zero, whereas that of a monolayer is finite (Jaihnig, 1984).
The predictions of this theory were in good agreement with
experimental results on the equilibrium surface pressure of
a monolayer in exchange with vesicle bilayers in the subphase (Schindler, 1980). Hence, although the surface tension of a bilayer membrane is not accessible directly, indirect measurements support the notion that it is zero.
White (1980) pointed out that the surface area is not
necessarily the only variable that may change when a membrane tries to minimize its free energy. The volume of the
membrane may also change, so that the free energy must not
be minimal with respect to the area, i.e., the surface tension
must not vanish. This implies a coupling between the area
and the volume, which is weak, however, because a lipid
molecule may expand laterally and shrink vertically while
Received for publication 15 December 1995 and in final form 20 March
1996.
QDr. Jiihnig died June 16, 1996.
Address reprint requests to Dr. Fritz Jdhnig, Max-Planck-Institut fur Biologie, Abteilung Membranbiochemie, Corrensstrasse 38, D-72076 Tiubingen, Germany. Tel.: 49-7071-601238; Fax: 49-7071-62971; E-mail:

jaehnig@piaf.mpib-tuebingen.mpg.de.
C 1996 by the Biophysical Society
0006-3495/96/09/1348/02 $2.00

keeping the volume constant. In essence, this happens at the

lipid phase transition, the area changing by 20-30%, the
volume only by 2-4%. Thus, for many purposes volume
changes may be neglected, leaving the area as the relevant
variable. Other variables that may permit the membrane to
find an energy minimum at finite surface tension are the
particle numbers of lipid molecules and associated water
molecules. The first case pertains to black lipid membranes,
which are in contact with a reservoir of lipid molecules at
their boundary, the second to membranes that are not saturated with water. In these cases, a finite albeit small surface
tension may exist.
The vanishing of the surface tension of a bilayer membrane may be understood by considering a membrane sheet
in stacks of membranes at excess water or the membrane of
a vesicle that is large enough that curvature effects can be
neglected. If the surface tension for a given packing density
were finite, because of attractive interactions between the
hydrocarbon chains (arising mainly from their hydrophobic
effect) the energy of the membrane could be lowered by
reducing its area. Such a shrinkage is possible because the
membrane is dispersed in water and free to compress or
expand. Hence, the membrane will shrink, but not infinitely,
because of repulsive interactions between the headgroups
(steric repulsion between the hydrated headgroups and/or
electrostatic repulsion between the charges on the headgroups). Actually, the membrane will adopt a state in which
the attractive interactions between the hydrocarbon chains
and the repulsive interactions between the headgroups balance each other. This is the case when the free energy is
minimal with respect to the area of the membrane, i.e., when
the derivative of the free energy with respect to the area
vanishes, the surface tension is zero and the bilayer membrane has adopted a state with optimal packing of the lipid
molecules.
The situation is different for a monolayer membrane
spread at an air/water interface. Even if the packing of the
lipid molecules is optimal so that the surface tension at the
lipid/water interface vanishes, a finite surface tension arises
from the lipid/air interface. Because the hydrocarbon chains
are in contact with air, the surface tension is that of a
hydrocarbon/air interface, which is -30 dyn/cm (Nagle,
1980; Jiihnig, 1984). This value is in good agreement with
the experimental result for the surface tension of a fluid
monolayer at optimal packing of the lipids (Schindler,
1980).
The first molecular dynamics studies of bilayer membranes were performed by van der Ploeg and Berendsen
(1983), who had already mentioned that the surface tension
should be zero. Actually, in their studies they obtained a
finite surface tension because they simulated a bilayer mem-

Jahnig

Surface Tension of a Lipid Bilayer Membrane

brane in vacuum. In this case, the steric repulsions between

the headgroups are too weak because of the lack of hydration and the attractive interactions between the hydrocarbon
chains are too weak because of the lack of the hydrophobic
effect. If the two effects do not balance each other, a finite
surface tension may arise. In more recent studies of Egberts
et al. (1994) and Tu et al. (1995), bilayer membranes in
water were simulated at zero surface tension (by imposing
an isotropic pressure of 1 atm). Good agreement with experimental data was obtained, which demonstrates that the
inclusion of a finite surface tension as in the work of Chiu
et al. (1995) and Feller et al. (1995) is not required. Direct
comparison of membrane simulations with and without
surface tension performed by Tieleman and Berendsen
(1996) revealed no significant differences.

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de Gennes, P. G., and M. Papoular. 1969. Volume jubilaire en l'honneur de
A. Kastler. PUF, Paris.

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